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The usual agroecological practices for preventing soilborne disease are well known: crop rotation, addition of organic matter and compost, sanitation of tools and plant materials, promotion of good soil structure, prudent water management, use of resistant varieties. Add to that list an incongruous entry — continuous monoculture. When the same crop gets hammered by the same disease in the same field year after year, once in a while the disease will suddenly disappear for good. This is the phenomenon of suppressive soil, and Daniel Schlatter and colleagues recently summarized the latest research on it.

While continuous monocropping contravenes good agroecological management on many levels, the appearance of disease suppression actually does arise out of agroecological principles. What we call disease is really the interaction between a host, in this case a crop plant, and a pathogenic organism. And whenever an organism is present in a field, it is subject to ecological forces. A field that contains a large population of a single species, whether it be a plant, insect, or microbe, potentially presents a target for another organism. For a plant, the opportunistic organism could be an insect or a fungus. For a microbe responsible for a crop disease, the opportunist could be an antagonist — a sort of armed competitor — or even a hyperparasite.

To be sure, a certain amount of disease suppression can come from enrichment of soil organic matter. Schlatter et al. differentiate this phenomenon as general suppression, the suppression that prudent organic farmers enjoy, whereby most soilborne diseases can cause only the most minimal damage. The other kind of suppression, that which arises from monocropping, is designated as specific suppression, where a specific disease caused by a single organism is the only one affected. Specific suppression can often be introduced into a field by addition of a small amount of already-suppressive soil. In addition, specific suppression requires the continuing presence of the host crop. If the field is rotated to a different crop, the resistance subsides, and it takes a season or more to return when the host crop is re-planted.

General suppression is thought to operate based on high numbers and high diversity of microbes present in the soil. This kind of microbial community insures that organic compounds are quickly broken down and taken up. Among these compounds are the exudates that a root characteristically gives off as it extends through the soil. It is these exudates that trigger pathogens to begin their attack. If the exudates dissipate immediately after release, the root may essentially slip past the pathogens unnoticed.

Regarding specific suppression, the authors of the review examine the mechanisms by presenting three case studies highlighting a continuum of suppression, from completely specific to somewhere between specific and general. The first regards the disease known as take-all of wheat. This disease is caused by a fungus that severely rots the plant’s roots. Certain strains of bacteria suppress the disease, and all of these turn out to produce an antibiotic known by the acronym DAPG. When these strains reach high population levels, the take-all pathogen is completely incapacitated and the disease disappears. The wheat plant’s roots even exude compounds that promote colonization by the DAPG strains. However, the DAPG producers have no effect on other pathogens.

The second case is that of Rhizoctonia bare patch of wheat and sugar beets. There is evidence that the organisms antagonistic to the Rhizoctonia fungus possess a certain amount of cross-antagonism against other pathogens, but the bare-patch-suppressing microbes are the least well characterized of the three case studies.

The third case is that of potato scab, a disease caused by a strain of Streptomyces, a genus of bacteria perhaps better known as the source of the antibiotic streptomycin. Interestingly, the antagonistic organisms are also strains of Streptomyces. It seems that the potato plant’s exudates are a food source for a suite of highly similar organisms, and niche theory predicts that in such a situation the best competitor will win out. In this case, the various strains of Streptomyces boost their competitive abilities in the presence of this limited food source by producing unique antibiotics that kill off their competitors. A casualty of this antibiotic arms race is the strain that causes the scab disease.

This third case of specific suppression is the closest to general suppression, although the mechanism is different from the fast degradation hypothesis. The cocktail of antibiotics pulsing through the soil can serve to eliminate other pathogens besides the bacterial strain responsible for potato scab. In fact, disease-suppressive Streptomyces strains can sometimes be enriched in the soil by incorporation of certain organic amendments, such as rice bran or the mustard family plant wall rocket, the presumption being that a particular type of food will cause the microbes that are able to digest it to fight over it, launching their specialized chemical weaponry as the competition intensifies. Whichever management practice initiates the chemical warfare, once it starts, it may tilt the microbial community composition toward ever stronger competitors, leading to a self re-enforcing dynamic that in some cases leads to lasting suppressiveness even when the original crop or amendment is gone.

Disease suppression has long been a phenomenon that emerged from the black box that is the soil microbiome. New tools for microbiome research are beginning to shed light on the inner workings of that system, and Schlatter and colleagues enumerate some of the methodological considerations for further advances. They also call for additional studies that use the knowledge that has been gained about suppression mechanisms to further our understanding of the agroecological circumstances and the specific management practices that will enhance disease suppression. For instance, will tillage increase or decrease disease-suppressive Streptomyces? Co-author Linda Kinkel invokes niche theory in predicting that no-till might allow the different strains to begin to coexist and to ease up on the competition, while tillage would disrupt any coexistence dynamic and more likely set off a chemical arms race. Would that happen in the real world? In every situation? Only field research, with a boost from microbiomics, will give the answer. For the foreseeable future, though, continuous monoculture remains a questionable bet for sustainable agriculture.

As if you needed any more evidence that microbiomes matter, wife-and-husband team Caroline Roper and Philippe Rolshausen have given us a microbiome study around the phenomenon of grapevines that escape Pierce’s disease.

 

Winegrapes as a crop are uniquely susceptible to diseases due to their propagation method.  Existing grape varietals such as Cabernet Sauvignon, Chardonnay, and Zinfandel are relics from the eighteenth century or earlier, kept alive through cuttings that are grafted onto more robust rootstocks.  They cannot be bred for disease resistance due to consumer rejection of hybrid varietals.  In France it is even illegal to breed with traditional grape varietals.  Grapevine pathologists are thus always assured of a job.

 

Pierce’s disease is caused by the bacterium Xylella fastidiosa, the “hard-to-grow xylem vessel-dweller”, Xf for short.  The bacterium gets injected into the water-conducting vessels of grapevine and other hosts, where it forms a film on the inside of these microscopic channels.  It was thought that the bacteria build up to such high numbers there that they block the flow of water to the leaves and cause scorching.  However Hossein Gouran showed in his Ph.D. research that the bacteria in the film are not the life stage associated with the scorching.  Rather, it is the free-floating stage of the bacteria that induces the actual disease.  These cells that have broken free produce an enzyme that flows up the xylem vessels and attacks the cells in the leaves, causing the scorch symptoms.  This revelation is so new that Roper and Rolshausen do not acknowledge it in the introduction to their study.

 

Pierce’s disease has long been a minor nuisance in California’s grape-growing regions, showing up on field margins that are near streams.  The native sucking insect known as the blue-green sharpshooter picks up the bacterium in the wild streamside vegetation and then disperses into the nearby grapevines, where it feeds on green stems.  It inserts its mouthparts into the xylem vessels, where it injects the bacterium as part of its feeding behavior.  The leaves on that segment of stem are the ones that show symptoms, but after the leaves drop in the fall and the vine has undergone a chilling period, it can emerge pathogen-free in the spring.

 

If that were the end of the story, it would be a mere footnote in the litany of diseases of grapevine.  Now, though, the introduction of the much larger glassy-winged sharpshooter from the southeastern US into southern California has given the Xf bacterium the upper hand in that region’s grape industry.  The new insect can inject Xf into the woody tissue of the grapevine, causing a much more devastating infection, and it avoids wild vegetation, instead moving extensively through the region’s orchards and vineyards.  Entire vineyards fail because of Pierce’s disease, and in northern California grape-growing facilities one can find wanted posters showing hideous blowup photos of the glassy-winged sharpshooter.

 

The real footnote of this disease story is that in vineyards that are ravaged by Pierce’s disease, occasionally there will be a lone grapevine that has escaped the disease.  This surprise cannot be the result of genetic resistance because all the grapevines in the vineyard are clones of centuries-old varietals.  With microbiome research all the rage, Roper and Rolshausen and their research groups asked if there was something about the microbiome of the escaped vines that protects them from Xf.

 

Serious microbiome research has only become possible with the development of so-called “next-generation” DNA sequencing technologies, new methods of reading off millions of DNA sequences in parallel.  The sequence is the order of the four possible building blocks of DNA, strung together in long strands to form a code that a cell can read for its instructions.  Roper and Rolshausen used one such technology, the Illumina system, where the millions of DNA segments get anchored to a tiny surface for a microscopic light show.  Since a DNA strand is made up of two halves that fit together perfectly, when one half is removed it can be recreated based on the sequence of the other half.  By monitoring the construction of the missing portion, one can determine the sequence of both halves.  Every new DNA building block that the Illumina machine adds generates a tiny flash of light from each anchored segment, with a different color representing each of the four building block types.  The sequence of colors in the series of recorded images corresponds to the sequence of a DNA strand at a particular spot on the surface, and given the millions of sequences recorded, with some computation the entire sample’s DNA sequences can be characterized.

 

The Illumina technology is useful in microbiome work thanks to DNA barcoding.  There are a few genes that are universal, contributing to a microbe’s basic cell structure and functioning.  In particular, the genes for the ribosome are indispensable, comprising the main part of the machinery for reading the DNA code.  They vary hardly at all from microbe to microbe because the vast majority of possible changes would be lethal.  This consistency makes these genes easy to find in the jumble of DNA.  However, there are segments in the DNA of these genes that do not get used in the ribosome, and therefore are free to mutate without consequence.  Different mutations are carried by different lineages, and the resulting DNA sequences can allow a researcher to distinguish different groups of microbes.

 

Roper and Rolshausen extracted the sap from symptom-free vines in southern California vineyards ravaged by Pierce’s disease and in northern California hotspots of Pierce’s disease and used ribosome DNA barcodes to compare the sap microbial community to that of the sap from nearby vines that had succumbed.  They looked at both bacteria and fungi, and while some of the fungi they found were interesting, there were too few to pick out a consistent trend between symptomatic and asymptomatic vines.  The bacterial communities were indeed different, although not nearly as rich as the bacterial community of a soil or a human gut, and the researchers mentioned a lot of the bacterial groups found, using the Latin, for anyone who is interested.  The key finding was that asymptomatic vines were low in Xf but had a high level a certain bacterial strain called Pseudomonas, which is known to have biocontrol properties.  Is this the key factor allowing the vines to stay healthy?  More research is needed.

 

With a strain of bacteria able to protect grapevines from Pierce’s disease, conventional ag research’s aim would be to commercialize the strain, with the hope of allowing private laboratories to make a profit by providing vineyard owners with another specialized input.  The high-margin winegrape-growing corporations would in turn be able to increase profits by extracting higher yields from their centuries-old relics, while any artisanal grower without the means to inject all her vines with a specially formulated bacterial preparation would be economically disadvantaged.  By contrast, the aim of agroecological research would be to seek management techniques that any grower could use that would increase the resistance of the vines to Xf.  This would be in the context of promoting overall agroecosystem health and community benefit.  I would even surmise that if varietals bred for disease resistance were ever to find acceptance, it would be by wine club members dedicated to small agroecologically managed vineyards.  More agroecological research is needed.

Plant breeders face a conundrum when it comes to plant diseases. The most powerful disease resistance genes, if not managed well, will quickly become useless.

Plants have an innate immune system that recognizes certain molecules that are typically found on pathogens. When a microbe presenting a typical molecular signature enters a plant, the plant basically bleaches the area using highly reactive oxygen compounds. The plant then activates genes that insure the microbe will not spread. However, successful pathogens overcome the innate immune system using molecules called “effectors” that disable components of the plant’s detection or response system.

The story does not end there, though. Thanks to Darwinian evolution, plant populations can develop resistance to pathogens. A dramatic form of resistance is the so-called R gene, the major resistance gene. If a pathogen possessing a single potent effector arrives, it will run rampant in a population of its host species. However, natural plant populations are typically very diverse. Any individual plant that happens to have an R gene that matches the pathogen’s effector allows it to recognize the effector and turn on its so-called hypersensitive response. Microbes with effectors are considered so dangerous that the plant will go crazy bleaching the point of entry until all cells in the area, pathogen and host, are dead. The result is an inconspicuous dot of dead tissue that shows where a pathogen attempted penetration.

In a natural population, the plant with the R gene will outlive its susceptible neighbors and pass this gene on to its progeny. In agriculture, this type of gene is highly sought by breeders aiming to develop resistant crop lines. A field of plants with the R gene will stand firm against the onslaught of a pathogen, growing robustly and giving their full yield where susceptible plants would turn out stunted, discolored, deformed, or dead.

In a further turn of evolution, however, the pathogen population can include individuals with a novel effector gene that allows them to disable a plant’s R gene and carry out its invasion of the plant’s tissues. These individual pathogens will reproduce thousands of progeny that are able to infect all the resistant plants. The pathogen has broken through the resistance. This is a common event, as a pathogen’s lifestyle depends on infecting plants, and therefore it is built to evolve new effectors quickly.

Another type of resistance is partial resistance, termed QTL, for Quantitative Trait Loci. In this case, instead of a single gene in the plant that acts as a tripwire for the pathogen’s effector, the plant has various traits that make it harder for the pathogen to carry out its lifecycle. Perhaps the plant’s external surface is harder for the pathogen to traverse, or one of the plant’s targeted enzymes is only partially disabled, or the plant produces a metabolite that slows the pathogen’s growth. Any single gene for partial resistance buys the plant only a partial or temporary escape from the ravages of the disease, but if many of these genes are present in an individual, that individual can be as resistant to the pathogen as if it had the appropriate R gene.

As you can imagine, partial resistance genes are more work for plant breeders. The QTL-resistant crop varieties they release must have multiple genes bred into them, or “stacked”. There is an advantage, though, in that the odds of any pathogen individual having enough genetic mutations to overcome all the resistance genes is essentially zero. In fact, breeders could stack multiple R genes in the crop varieties they release as well and enjoy the same odds against breakthrough, but expediency often overrules prudence when disease threatens. Furthermore, if one breeder expends the time and resources to stack R genes while other breeders release varieties with single R genes, the pathogens may break through the single R genes one by one, and the crop line with the stacked R genes may end up with few or just one functioning resistance gene. In that case, the pathogen population may be only one mutation away from breaking through the stack.

Plant pathologists are thus perennially concerned about release of resistance genes in seeds to farmers, but releases are often out of the control of the plant pathology commmunity. The network structure of plant pathologists, breeders, non-profit germplasm repositories, agribusiness corporations, and farmers presents a complex adaptive system where each actor has its own incentives, all of whom interact to produce the dynamics of resistance gene diffusion across the globe, both prudent and expedient. Karen Garrett and her plant pathology and plant breeding colleagues have looked into these dynamics using an epidemiological approach, published recently in Phytopathology.

Garrett et al. examine network structure for four staple crops: cassava, potato, rice, and wheat. The result is four abstract diagrams, evocative respectively of a double spiderweb, the tentacles of a sea anemone, a time-lapse photo of flocks of birds taking flight, and spaghetti with cheese flowing off a plate, all with colorful circles and squares on the periphery and black ones in the center. The central black circles show the centrality of the non-profit International Agricultural Research Centers, the IARCs. The other colors are codes for the continents where the different actors are located. Arrays of black squares represent private multinational companies, clustered near the center for potato and wheat, less obtrusive for cassava and rice.

The dots and squares on the periphery are segregated by color, signifying a dearth of direct connectivity between continents or regions. In terms of resistance gene diffusion, this means that there is no easy way for resistance genes from one continent to be bred into another continent’s crop, potentially leaving some areas without optimum disease protection. However, from the perspective of pathogen evolution, it could be helpful to have different resistance gene profiles in different regions to reduce the likelihood of the emergence of a super-strain able to infect the entire world crop. Also, less movement of the plant material containing the resistance genes means less likelihood of bringing hitchhiking pests and pathogens to new regions.

The reason for the four diagrams’ different arrangements of black squares — representing the international-scale private breeders — is the privileged position of some of their non-profit counterparts, the IARCs. In the case of cassava, a staple in tropical Africa and Latin America, the entire network is small, making the lone black square look rather incongruous and with very few connections. Private corporations seek out crops with the largest markets, and cassava is not one of them. In the case of rice, the authors explain that the international centers have played such a dominant role in the development of major resistance genes toward bacterial blight and rice blast diseases that there has been little profit incentive for the entry of private companies into the network. On the opposite extreme is wheat, for which several multinational corporations have extensive germplasm collections and have highly connected black squares in the network diagram. For potato there are similarly black squares in a more central position, but a closer look also reveals a proliferation of red squares on one side of the abstract anemone, representing a large number of private interests in wealthy Europe.

The abstract diagrams and their underlying analysis is a work in progress. The idea is to provide insight into what-if questions, such as how resilient a network would be if a major hub should disappear, such as the recent abandonment of the seed collection at the International Center for Agricultural Research in the Dry Areas in Aleppo, Syria (the Center was reconstituted in Lebanon and Morocco with backup seeds from the Svalbard vault). This type of change in a network would be unfeasible to test in an experiment, but past performance of the existing networks in terms of R gene diffusion and lag times can provide insights into the robustness of the complex adaptive system, as well as whether the networks themselves can be shaped by institutions embedded within them, e.g. the IARCs.

An observation by the authors is that private breeders tend to weaken the structure of the overall network. Whereas non-profit breeders’ focus is on providing farmers with plant material containing resistance genes, and ideally getting feedback on their performance from the farmers, private breeders have an incentive to hoard crop germplasm resources and release only those resistance genes that will make them a profit. Because of pro-corporate intellectual property laws and the development of biotechnology and hybrid varieties, private breeders are proliferating. The authors point out that private breeders focusing on more profitable markets enjoy a funding advantage for research over the constrained resources of the international research centers, thus allowing them to more quickly coordinate the release of resistant material. Poorer farmers have derived some benefit in the past due to trickle-down effects of resources originally directed at richer farmers.

A response to the privatization trend is the rise of open-source breeding movements, but the authors are unable to evaluate the effect of these efforts on breeding networks. Another shortcoming of the analysis, and of the underlying networks themselves, is the emphasis on staple crops. Traditional agriculture depended on a dizzying diversity of crops that is hard to fathom from the perspective of modern agriculture. This diversity provided an economic resilience to farmers as well as environmental services that benefited the crop plants, both of which have been replaced in modern low-diversity agroecosystems by continuous subsidies, in forms that range from pesticide development to resistance-gene prospecting to famine relief. A research focus on a handful of crops has promoted this low diversity, to the detriment of not just the environment but also human diet. While a big-picture analysis of the diffusion of resistance genes is an improvement over uncoordinated efforts to fight local outbreaks or to make a profit, such analysis must also be viewed as a small piece of the overarching big picture that is agriculture.

The story of a single rhizobium bacterium making its way into a legume root where it fills a nodule with its nitrogen-fixing brood is not as simple as once thought (see my previous post for background). The soil is full of bacteria, and it should be no surprise that other species get into the nodule along with the nitrogen fixer. Also, given the way that bacteria swap genes, it is little surprise that unusual species get hold of nitrogen-fixing genes, and even nodule-inducing genes. Martínez-Hidalgo & Hirsch have just come out with the latest compilation of the nodule microbiome in the new journal Phytobiomes.

Of course the predominant inhabitants of a nodule are the nitrogen-fixing bacteroids, thanks to the strong control the host plant exerts over the nodule environment. Some of the other inhabitants, though, are also beneficial to the plant. The ways they can help include solubilization of phosphate, production of compounds that solubilize iron, protection against heavy metal toxicity, possession of antifungal activity, and other plant growth promoting attributes. Some companion bacteria produce plant hormones that increase plant growth, although I have not heard a convincing argument as to why a plant is not equally benefited by producing its own hormones. Co-inoculation studies involving nodulating bacteria paired with other nodule inhabitants have shown benefits such as increases in nodule number & weight, plant nitrogen, dry shoot weight, pod weight & number, pathogen resistance, seed weight, and total yield.

Some bacteria with plant growth promoting capabilities have picked up genes for nitrogen fixation or nodule induction the way that bacteria are known for picking up new genes. Bacteria can receive genes from closely related bacteria through conjugation, AKA bacterial sex. Under favorable circumstances they can also take up DNA from dead cells in the environment and incorporate it into their own complement of genes. Nitrogen fixation requires a gene dubbed nif, and the ability to communicate with a plant and negotiate growth of a protective nodule requires another gene, called nod, both of which can only come from a strain that already has such a gene. Heavy-metal-resistant strains of nitrogen-fixing Cupriavidus picked up their nif and nod genes from the related species Burkholderia. A strain of Pseudomonas, a genus more commonly associated with diseases of plants and humans, was discovered nodulating black locust using a nod gene received from the more commonly nodulating bacterial species Mesorhizobium. A strain of Klebsiella, a genus associated with opportunistic infections in humans, was found in nodules of several legume species and was demonstrated to nodulate fava bean in a laboratory setting.

The authors envision widespread co-inoculation of legumes with nodulating bacteria and beneficial companion bacteria. While biological fixation of nitrogen has environmental benefits over industrial fixation, the model of turning scientific discoveries into products has its own downside. Highly capitalized farmers will be able to buy any input that can increase their profit margin, while farmers who are struggling financially will have to cut costs and instead use knowledge and additional labor to substitute for external inputs. Scientific knowledge that can only be accessed by specialized corporations will tend to accrue benefits to those who are already better off. If co-inoculation technology is to benefit those most in need, a system of public production and distribution of inputs would be necessary.

The authors point out that co-inoculation would be particularly helpful in degraded soils. Certainly the restoration of microbial diversity would contribute to restoration of soil to a healthy state. It would be helpful, though, if scientific investigations could zoom out from the reductionist business of characterizing beneficial co-inoculant species and in addition elucidate environmental conditions and management practices that would promote the proliferation of in situ populations of beneficial nodule-inhabiting companion bacteria. Laboratory cultures require time, labor, resources, and paperwork to ship internationally, but knowledge can move around the globe in an instant. The era of purely reductionist science must yield to whole-system perspectives. In this way, basic research, such as molecular microbiome studies, can help reduce economic inequality rather than contribute to it.

It seems I have a fascination with legumes. I was about to pass up the New Phytologist journal’s booth when they handed me a reprint of the recent (2017) review by Sprent, Ardley, and James on legumes. Before I read this article, if you had asked me what a typical legume is I probably would have answered “beans”. However, as the third largest plant family, the legumes present a kaleidescope of forms, most of which are not your garden variety.

The legumes are defined by pods that open up along both edges, labeled by botanists as “loments” or “legumes”. Many legumes host nitrogen-fixing bacteria, but many do not, and not all plants with nitrogen-fixing partners are legumes. In my classes I learned that there were three subfamilies — or maybe four — that were classified according to their flower type. One subfamily was characterized by flowers that are pattered like those of the pea, with a large petal at the top giving the appearance of a bonnet, the other petals forming something like a beak in front of it. An early botanist had the impression of a butterfly when he saw this type of flower and called it papilionoid, and thus the subfamily with this type of flower became the Papilionoideae. A second subfamily had flowers with five more-or-less equal petals, sometimes with “claws”, and with a slight bilateral symmetry, such as those my grad school advisor had studied in the tropics. Her connection to these species left me with certain regard for this group, the Caesalpinioideae, named in honor of another early botanist. The third subfamily had flowers with no petals, only stamens and pistils, that clustered together into fuzzy puffs such as those on an acacia, a group named the Mimosoideae, evoking a certain brunch cocktail. The fourth group designated as a legume subfamily had been recognized as a separate family by the time I learned of it.

Part of the reason that legumes are so successful, and the reason they are important to humans, is their ability to harbor specialized bacteria that turn nitrogen gas into nitrogen fertilizer, a process known as nitrogen fixing. The bacteria benefit from this arrangement because they are fed and protected inside the legume roots, while the legume gets millions of tiny internal fertilizer factories. In another one of my classes I was taught how the plant sends a chemical signal into the soil that attracts the bacteria. The bacteria respond with their own chemical signal, causing the plant root hair to curl around a single bacterium and open up a narrow tube, called an infection thread, for the bacterium to enter. The bacterium travels into the main part of the root, where it multiplies as the plant builds a nodule around it. The plant releases the bacteria into a specialized compartment, where they become nitrogen-fixing zombies called bacteroids that have lost the ability to divide, often becoming unable to live in the soil again once the root dies and the nodule breaks open.

Sprent, Ardley, and James have updated my understanding of legumes and nodulating bacteria. The agricultural legumes we are familiar with, especially those grown in temperate zones, are biased toward European and Middle Eastern species such as alfalfa, clover, vetch, and peas, which have been exported around the world. In other parts of the world, by contrast, legumes are often trees or shrubs. The textbook infection-thread story is just one mode of nodulation. In some legume species the infection thread does not end up anywhere, becoming a “fixation thread” as the bacteroids start performing their nitrogen fixation inside the tube. In other legume species the bacteria enter through the root epidermis, and no infection thread is formed. This is the mode in the lineage that includes Scotch broom, rooibos, sunnhemp, and lupine, the latter being noteworthy for its wraparound nodules. Finally, some legume species allow bacteria to enter through cracks. A semi-aquatic West African Sesbania species grows nodules in this way — on its stem.

The previous classification scheme has been overturned, as evidence from DNA has shown that the Mimosoideae are actually a branch of the Caesalpinioideae. Furthermore, some members of the Papilionoideae have perfectly radially symmetric petals, giving the impression of a hibiscus flower. All of the African “acacias” are now placed in separate genera (sing. genus) from the Australian genus Acacia. And even though I had an image of caesalpinioids as tropical trees, the genus Chamaecrista includes temperate zone species and annuals, such as partridge pea, a North American native used for forage.

Another principle I learned from classes was that a species of nodulating bacteria is specific to a legume host genus. The specificity may be very strict — soybean will not nodulate in North America unless the soil is inoculated with the bacterium Bradyrhizobium japonicum. This trend does indeed hold widely across the legumes, particularly those widely exported European/Middle Eastern species. However, among Mimosa species, it is soil factors that determine the symbiotic bacterial species. Sometimes when a legume plant genus is distributed between different continents, its various member species adapt to whichever class of nodulating bacteria is present on the respective continent. There are also legume species that are “promiscuous”, such as the common bean, that can nodulate with bacteria belonging to the distantly related classes.

One mechanism for host-bacteria specificity seems to be a result of evolutionary arms race dynamics. The species of legumes in the European/Middle Eastern group produce a suite of antimicrobial-like molecules that regulate the process of turning free-living bacteria into highly efficient and subservient bacteroids. Each bacterial species, for its part, produces a unique enzyme that neutralizes a range of these regulatory molecules. On the one hand, the enzyme can allow the bacterium to multiply more successfully in the plant and get away with fixing less nitrogen. On the other hand, the particular set of regulatory molecules that the enzyme neutralizes will determine which hosts it can exist within.

Another factoid from the classroom is that some legumes are capable of producing potent toxins. A lecturer told of an acquaintance who cooked and ate scarlet runner bean roots and had to have his stomach pumped. Someone else became ill from munching on a single raw scarlet runner bean while working in her garden. Raw kidney beans can cause nausea with the ingestions of single-digit quantities. Consider, though, the southwest Australian leguminous shrub genus Gastrolobium, which produces fluoroacetate, a cell respiration inhibitor so toxic as to eliminate a sheep after just a few bites. Evidently the endemic legumes of this area share an unusual class of toxins that are not alkaloids and do not incorporate nitrogen atoms at all. Perhaps this attribute is related to their adaptation to low-phosphate soils, phosphate being crucial in most legumes for the nitrogen fixation process.

Some lineages of nodulating bacteria have given rise to well known pathogens. Agrobacterium, associated with crown gall, was revealed to be part of the genus Rhizobium. Agrobacterium uses a small circle of DNA separate from the main chromosome to carry its infection genes, just as nodulating Rhizobium species use a separate DNA circle for their nodulating genes. Another genus, Burkholderia, is known for several pathogenic species causing blights and spots on crops and ornamentals, and only fairly recently was discovered to include nodulating species found in South American mimosoids and South African papilionoids.

The different classes and genera of nodulating bacteria are often associated with particular environments. For instance, Burkholderia species prefer acidic soils and higher altitudes, whereas in higher-nutrient soils they are outcompeted by other species of nodulating bacteria. Other genera are associated with seasonally dry acidic soils or with alkaline soils. The genus Cupriavidus is known for heavy metal tolerance. However, strains of Rhizobium can be found in many environments.

A couple more factoids: Although the soybean, Glycine max, is native to China, oddly the genus Glycine is most diverse in Australia. And aside from providing nitrogen, nodulation may be beneficial in other ways, such as improved water use efficiency. I wonder how this benefit would figure into Ford Denison’s analysis of “cheater” strains. Myriad other factoids are presented in the review that only a legume researcher could love. If you know what “mirbelioid” means, you are the target audience. The value of knowing the full diversity of the legumes, according to the authors, is to help in the search for legumes adapted to extreme conditions for use in agriculture under a changing climate. I would also add that new agricultural legumes would be useful if they have resistance to diseases of today’s set of forage and green manure legumes.

So what is a typical legume? The legume genus Astragalus, made up of herbs and small shrubs, the milkvetches and locoweeds, contains something like 2,500 species, the most of any plant genus, but it is hardly representative of the legume family. I would have to say that this is another instance of a short question with a long answer.

So organic is the new conventional.‭ ‬So voting with your dollars will not challenge the neoliberal order.‭ ‬What,‭ ‬then,‭ ‬is the path to sustainable agriculture‭? ‬Connor Fitzmaurice and Brian Gareau got down into the weeds‭ ‬–‭ ‬literally‭ ‬–‭ ‬in search of possible answers,‭ ‬and they present hope and direction in their book Organic Futures.‭ ‬In what‭ ‬reads like an extended response to Julie Guthman‭’‬s political economy analysis of organic agriculture,‭ ‬Fitzmaurice and Gareau give us a cultural anthropology study of some of the people who are forging an alternative to Big Organic.

Organic farming has gone from an alternative agriculture movement to a big business,‭ ‬with big growers hewing to the letter of the law while‭ ‬disregarding environmental,‭ ‬economic,‭ ‬and social sustainability. Yet‭ ‬there are still organic practitioners who reject the profit motive and seek to live out the values of the original movement.‭ ‬These are small,‭ ‬predominantly younger farmers who rotate crops,‭ ‬grow a diversity of cultivars,‭ ‬plant hedgerows,‭ ‬sell locally,‭ ‬and even question the USDA list of allowed chemicals.‭ ‬They are subject to the supremacy of market forces that‭ ‬constrain us all,‭ ‬but they have carved out their own space where they can put at least some of their ideals into practice.‭ ‬It is this tension between the structural and the personal that Fitzmaurice and Gareau explore with their ethnographic portrait of one small New England organic farm.

Regarding the very idea of a New England farm, an idea that might induce images of stubborn old-timers eking out a pitiful yield on rocky soil during a two-month growing season, Fitzmaurice and Gareau point out that New England farming is actually quite productive, with yields comparing favorably to those in the rest of the US, but that the fractured landscape is not conducive to the kind of big agribusiness that dominates in places like the Midwest and California. The farmers are younger, reviving the region’s agriculture after farming there came to seem unfeasible after Agriculture Secretary Earl Butz’s admonition to get big or get out. They are generally white and college-educated, a demographic that also includes a significant proportion of the farm workers there. They take advantage of a niche market where proximity to consumers and face-to-face interactions are valued.

The‭ ‬concept that Fitzmaurice and Gareau‭ ‬emphasize is that of matches.‭ ‬As small organic growers negotiate the demands of running a business with their concern for environment and community,‭ ‬they undertake many smaller negotiations with people and practices.‭ ‬When conscientious neighbors volunteer to help fill CSA boxes and get free produce as a gift of gratitude,‭ ‬that is a match.‭ ‬When‭ ‬a local restaurant appreciates the quality of the farm‭’‬s produce and makes a standing commitment to purchase part of the harvest,‭ ‬and in turn the farm gears part of its production to meet the needs of the restaurant,‭ ‬that is a match.‭ ‬When the farmer hires an‭ ‬environmental studies major with a vision of agricultural sustainability to work as a laborer,‭ ‬and then treats that laborer as a‭ ‬human being‭ ‬and a‭ ‬participant,‭ ‬that is a match.‭ ‬When the farmer uses a microbial preparation on the tomatoes to fight late blight in a wet year instead of turning to the more toxic — but organically permitted — copper spray alternative,‭ ‬that is a match.‭ ‬And when the farming couple rents out the cottage on their idyllic property to‭ ‬draw a substantial portion of their annual income in order‭ ‬to approach a middle-class lifestyle,‭ ‬that is a match.

These small matches are the everyday acts that reflect the larger‭ struggle between values, customs, lifestyle, and positive self-image on one side and the monetization of human interactions on the other. Farmers and farm workers often aspire to farming in an environmentally friendly manner and creating community. They value their connection to the outdoors. They have a need to see themselves as good people doing the right thing. However, Big Organic, largely from California, has driven down prices at the farm gate, all but wiping out the price premium that organic producers could count on to compensate for lower yields and higher expenditures on labor. Instead, the higher retail price of organic produce accrues to the intermediaries farther along in the food chain. The organic farmers profiled in the book have to depend on special circumstances to make a living, including inherited property with an easement that limits its use to agriculture and natural environment, farmer mentors, a zeitgeist where buying local is valued, personal connections to buyers and volunteers, and a non-farming source of income, not to mention one member of the farming couple having a knack for handling the organic certification paperwork.

‭One of key practices of the subject farm is their CSA, an acronym standing for Community Supported Agriculture. The practice entails selling season subscriptions to local consumers and then providing them with a weekly basket of whatever produce the farmers have to offer at that time. This arrangement provides up-front cash when it is needed at the beginning of the season, when farmers might otherwise have to take out loans. It benefits the environment by giving farmers extra incentive to plant a diversity of crops, and also giving them the ability to opt out of the use of chemicals if one of those crops should fail. It strengthens the community by bringing together neighbors who volunteer to help fill produce baskets on pickup day and giving subscribers at least some personal connection with the farmers. And it benefits the organic movement by occupying a niche that Whole Foods and Walmart have had difficulties moving into.

‭Fitzmaurice and Gareau detail the ways in which the profiled farmers take the extra effort to make their vision of organic agriculture work. They put in long hours planting, weeding, harvesting, packaging, record-keeping, negotiating. At one point they hand-pruned the flowers from a field of potatoes in order to keep bees from succumbing to the biopesticide to be used on the Colorado potato beetles. They pack extra turnips into a bunch to make a good impression on the CSA members. Perhaps most problematic, they forgo the comfort of the middle-class lifestyle that their education level might afford them and their children. Fitzmaurice and Gareau decry the disproportionate burden that small farmers must shoulder in bringing about a more sustainable agriculture.

‭From my agroecological standpoint, I paid more attention to the details of pest management than Fitzmaurice and Gareau with their sociological focus. Bt bacteria might have been the biopesticide used on the potato beetles. If so, there should have been no danger to bees visiting sprayed flowers, as the strain of Bt used on beetles would be beetle-specific. I cannot say for sure, as Fitzmaurice and Gareau do not name the biopesticide. Other pest problems on the farm included aphids on the chervil and hornworms on the tomatoes. The chervil was unsalvageable, and the more experienced member of the farming couple was considering interplanting flowers in the following year’s tomato crop to attract beneficials that might reduce the hornworm population. It is well known that more diverse vegetation reduces pest populations, and nectar sources in particular attract predators and parasitoids that kill pests. How unfortunate that young farmers with years of experience did not already know to intercrop flowers with their chervil and tomatoes. To me this was an indicator of lack of institutional support to provide education and training for farmers who strive to farm more sustainably.

‭In the end, Fitzmaurice and Gareau concede that Julie Guthman’s political economic analysis is correct. Under a neoliberal economic order, local organic produce is considered another niche market. Elite consumers make individual choices to consume status-symbol foods according to their preference, reinforcing wealth inequality, while the powerful economic players make allowances for such individualistic activity and continue to steamroll society with industry consolidation, downward pressure on wages, regulatory capture, defunding of public support for small farmers, increasing uniformity with the illusion of choice, and further exploitation of the environment. Fitzmaurice and Gareau’s philosophical answer is that any socioeconomic current that might eventually supplant neoliberalism will necessarily emerge as a component of the existing neoliberal order. As such, a movement of conscientious community-building farmers who create alternative socio-economic relationships (“matches”) might be the seed for an as-yet inchoate new economic paradigm.

‭As hopeful yet critical theorists, Fitzmaurice and Gareau make some recommendations, based on the Plentitude model‭. First is a transformation of the CSA model. The profiled farmers lamented that the CSA was not creating more community. The subscribers would show up on pick-up day, exchange a few words or hold a brief conversation, and then leave, never taking part in any of the actual farming activities. Fitzmaurice and Gareau envision a Community-Supported Community Agriculture, something perhaps akin to a community garden with professional farmers guiding it all. The consumer community would plant and care for the produce that they would harvest and eat, not in the atomized fashion that the carefully demarcated plots in existing community gardens necessitate, but as a rational agroecological whole.

‭Second is an extension of current farm-to-institution arrangements, such as farm-to-school programs. Students could go beyond enjoyment of fresh local produce by actually interning on local farms. They could earn credits for their efforts, and the institutional underwriting of such a program would provide support for the farmers and the community-building.

‭Third is an explicit inclusion of farm labor justice in organic certification, perhaps through separate third-party certifiers. Fourth is a stronger commitment by organic farms to environmental consciousness, from the number of trips CSA subscribers make to the farm, to tighter on-farm nutrient cycling and generation of energy, to cropping choices more suited to the local conditions than to consumer demand. Finally, movement organic agriculture must continually strive to remain alternative as Big Organic moves in to co-opt the innovations of sustainability, and the key to this is using community-centered development to counteract the power of money.

Anyone have other ideas?

Organic spinach has a big problem — downy mildew. Conventional growers have effective sprays for it, but organic growers rely largely on resistant spinach varieties. Unfortunately, new races of downy mildew that overcome spinach resistance genes are appearing every year.

Downy mildew is not a true fungus, but an oomycete, a relative of the potato late blight pathogen, the one involved in the Irish potato famine. There are hundreds of species of downy mildew, each specialized on one or just a few host plant species. Spinach downy mildew is not known to infect any other plant species besides spinach. The pathogen grows inside the leaves, causing them to yellow and wilt, and then it emerges from the stomates on the underside, giving a characteristic downy appearance. The soft downy portion produces spore-bearing structures anatomically characterized as sporangia (singular sporangium) that themselves break off and float through the air, acting as individual spores to propagate the pathogen.

Downy mildew is a problem not just for its direct effect on spinach leaves. Because organic spinach from California once had an instance of E. coli contamination that sickened many consumers, killing three, any infection of spinach is looked upon with suspicion by wholesale buyers, even that of a pathogen that cannot infect any plant but spinach, much less a human. Thus the threshold for rejection of an entire field of spinach is 1-5% infection with downy mildew. This low rate may help reduce the chances that a clamshell of spinach will turn to mush, but it makes organic spinach production a risky endeavor.

Dr. Robin Choudhury did his dissertation research examining the disease dynamics of spinach downy mildew. He studied aerial spore (sporangium) dispersal by means of traps with small sticky rods revolving around a pivot that capture everything floating through the air. Traps were located at points up and down California’s Salinas Valley, and the rods were changed out every few days during the course of two seasons. By extracting the DNA from everything stuck on the rods, Choudhury could test for the presence of downy mildew spores using a highly sensitive, highly specific technique known as qPCR. This technique amplifies a segment of DNA unique to the species of downy mildew from spinach, Peronospora effusa. By monitoring the amount of amplification necessary to detect the specific DNA segment, a researcher can also determine the number of spores captured.

With volumes of data on hand, Choudhury applied epidemiological analyses to find patterns. He found that the number of captured spores showed an exponential increase over each season. Furthermore, within that overall trend there were regular pulses of spores that may have corresponded either to pathogen generation time or to spinach harvest cycles. Either way, ever-present spores are bad news for growers.

In another sleight of analysis, Choudhury estimated the dispersal distance of the spores from an outbreak. Of course the farther a spinach field is from an outbreak, the fewer spores will arrive at it. The question is how far the spores will travel. According to Choudhury’s models, there is some likelihood that there is a limit to the distance that the vast majority of spores will travel, but there is a higher likelihood that a significant proportion of spores will travel very long distances, potentially endangering spinach fields in remote locations in the valley. These data were rather noisy, though, and did not completely rule out the former scenario. On the ground, Choudhury showed that an active outbreak would lead to a higher level of infection 5.6 meters away, but beyond that the infection rate was no different from the background rate.

Dr. Choudhury also did a trial of mixed varieties of spinach. The reason for mixing varieties with resistance to different races of a pathogen is twofold. For strictly market reasons, if one pathogen race takes out a variety, the remaining resistant varieties will still produce. A grower never knows which races will be present, and so will have to grow multiple varieties to insure a harvest. However, the current practice is to grow the different varieties separately in wide strips because the growers worry about inconsistencies in leaf traits. This arrangement misses out on the epidemiological benefit of growing the mix of varieties in a single bed.

If a field is full of plants that are genetically identical, then a single infected plant will give off spores that are adapted to every plant in all directions. However, with a good mix of varieties, the plant’s neighbors may all be resistant to those spores, and any spores that land on resistant neighbors will be subtracted from the total pool of spores available to spread the disease. This dilution of susceptible hosts can slow the spread of disease. The intercepted spores may even pre-arm the neighboring plants against races of the pathogen that are adapted to them, a phenomenon known as induced resistance.

Dr. Choudhury showed the growers his mixed-variety field and challenged them to point out non-uniform plants; they could not. Unfortunately, the trial was disappointing. Although few varieties succumbed to downy mildew, resulting in a lower-than-expected total disease incidence for a mix, the disease incidence still crossed the 1-5% threshold. It may be that there have already arisen too many pathogen races for this method to succeed. The only scenario where mixed-variety plantings might work would be if the method were widely adopted across the valley.

The reason that new races continue to emerge is that growers depend too heavily on a small number of varieties that are resistant to the known races. With the vast acreage of the Salinas Valley planted to just a few varieties, the fast evolution of the pathogen will generate races that are pathogenic on these varieties as well. One strategy to put the brakes on this fast evolution would be to discard seed lots with too many sexual spores of the pathogen. This type of spore is where a new genotype can be formed, and with enough new genotypes, a new pathogenic race can arise. However, the seed producers, who are located in states to the north, might not be willing to discard a portion of their product for the benefit of the Salinas Valley system.

A couple of practices that Choudhury was not able to challenge were planting density and irrigation. The demand for organic lettuce has burgeoned, and now the standard practice is to grow a high-density lawn of spinach on 80-inch beds that stretch off into the horizon. Spinach production fills a huge area of the Salinas Valley, nicknamed the nation’s salad bowl. The endless expanse of spinach is a giant petri dish for pathogens, and the crowding insures a continuously humid layer that promotes spore germination. To make matters worse, the growers overhead-irrigate, absolutely insuring excellent spore germination conditions.

Big organic growers have been lured by the profit motive to shift to an industrial mode of spinach production without regard to agroecological realities. In so doing, they created a downy mildew crisis, and they have called in the plant pathologists to deal with the problem. It makes one wonder how much of what plant pathologists do is simply trying to clean up the disasters of industrial agriculture. Large-scale organic spinach is just as industrial as conventional agriculture. Resistant varieties, perfectly timed biofungicide application, disease scouting, and hand roguing might get this season’s crop to market, but without an agroecologically sound system design, these measures may not save organic spinach production into the future.

“Feds Feed Families”. A key responsibility of the Federal Government is to assist those who struggle to make ends meet but occasionally come up short. That’s not what the Feds Feed Families campaign is about, though. No, it is campaign to encourage employees of the Federal Government to make individual contributions to food banks, with no dedicated expenditures of Federal funds beyond the tax deductions that are available to those employees who are fortunate enough to have bought a house and thus come out ahead if they itemize deductions.

It is well known that government employees are paid less than industry employees with comparable qualifications. The tradeoff is that government employees are supposed to enjoy more generous benefits and greater job security. Under the Obama Administration, Federal employees were subject to a freeze on cost-of-living adjustments so that Obama could pay for his extension of Bush’s tax cuts for the wealthy. When the freeze was lifted, the adjustment was modest — remember that this Administration expected Social Security recipients to make do with buying lower quality goods when prices rise. Now, under the Trump Administration, Federal employees are worried about job cuts, or if they keep their job, facing having to do more with less.

How unreasonable, then, to expect Federal employees to shoulder the responsibility of providing for less fortunate participants in the economy. In the wealthiest country in the world, which has seen steady economic growth for many years, John Boehner’s excuse that the Federal Government is broke is ridiculous. The money is out there, but the Government is committed to not using it.

To be fair, employees of the USDA have access to harvests that are not meant for sale, and these are included in the Feds Feed Families campaign, a praiseworthy effort to prevent food waste. Also, there is a procedure for employees with backyard gardens to donate their excess bounty to food banks, for which they are given a receipt for the cash equivalent of the weight of the produce donated, once again a tax break to those who can afford a house.

However, in a perverse twist to an already perversely named program, employees who want to make cash donations are discouraged from giving them directly to food banks. Charities often encourage donations of cash over goods because they can use the cash to leverage a higher value of goods than the donor could purchase with the amount of the donation. Instead of this, the employees are directed to make “virtual donations”, whereby they find a food retailer that is capitalized enough to offer online shopping, pay for some food, and direct that it be donated to a food bank. In this way, wealthy food retailers make a profit on employee donations. Given the pervasive wage-depression efforts of big food sector corporations, the donations will feed the forces that exacerbate food insecurity at the same time that they feed the food-insecure.

Individual charity will never fulfill all the needs of struggling families, especially when it becomes a vehicle for enriching the wealthy. The solution is economic equity. The Feds — meaning the Federal Government — should take responsibility for the well-being of the people.

Disregarding agroecological principles can lead to collapse. Florida citrus growers learned this lesson the hard way. Researchers in California are trying to prevent a rerun.

Huanglongbing, or HLB for short, is a disease of citrus that was originally recognized by farmers in southern China. It causes blotchy yellowing of leaves, sour deformed fruit, and — most devastating — premature fruit drop. The cause is apparently the bacterium Candidatus Liberibacter asiaticus (CLas), but as the incomplete italicization of the name indicates, this bacterial species cannot be grown in the lab, and therefore it has not been subjected to the steps necessary to confirm it as the pathogen. The CLas bacterium is transmitted to citrus leaves and stems by the Asian citrus psyllid, a tiny winged sucking insect similar to an aphid. The bacterium lives quite happily in the psyllid’s gut, but it can only be passed on to the insect’s offspring when they feed on an infected plant. This is where the citrus tree comes it.

The psyllid makes sure it injects some of its gut bacteria when it feeds on a leaf in order to provide its offspring with a meal of the beneficial bacteria they will need for survival, notably a species called Wolbachia. The CLas bacterium accompanies the Wolbachia, and in a fascinating case of bacterial genetics, can only survive in the presence of the Wolbachia. CLas at some point in its evolution was attacked by a virus that incorporated its own DNA into the bacterium’s DNA, and this internal virus is always poised to start replicating and burst out of the CLas cell, killing it. When scientists try to grow CLas in a Petri dish, this is what happens. However, in the environment where CLas normally grows, the virus is kept in check by a molecule that the Wolbachia produces. This psyllid-Wolbachia-CLas relationship has led researcher Georgios Vidalakis to call CLas a microbe of the Asian citrus psyllid, with citrus as just a transient host.

Once CLas is inside its transient plant host, it can spread only very locally within the plant, causing the leaves on just one branch tip to yellow. This gives a very patchy appearance of yellowing on a tree during the early stages of an epidemic. The only way that CLas can spread to the rest of the tree is when the psyllid juveniles grow up and fly to other locations on the tree, as well as other trees in the orchard. One unfortunate consequence for the localized distribution of the bacterium on the tree is that pre-symptomatic infections cannot be detected by monitoring programs that test tree sap unless the sap sample happens to come from a twig that is infected, and therefore there is usually widespread disease before the presence of CLas is confirmed.

The Florida citrus industry was slow to respond to the emerging threat of HLB disease. Where a comprehensive program for early eradication of the disease would have been an order of magnitude more costly than a program of strict quarantine to keep the disease out in the first place, once the disease becomes well established it is yet another order of magnitude more costly to try to manage it, in terms both of treatments and lost income. At this point Florida citrus production has fallen to the level of the 1940s. At least one commentator would like to blame the decline on venom from Anita Bryant, the 1950s-era singer who leveraged her fame to become both spokesperson for the Florida citrus industry and the leader of a nasty campaign to deny civil rights to gay people. Either way, there is a certain level of blame that the industry deserves.

What were the agroecological principles that were violated, allowing HLB’s destructive march across the state? Extensive monocropping allowed psyllids to move unimpeded from tree to tree, orchard to orchard, and county to county. A narrow genetic diversity insured that every citrus tree in the state is a susceptible host for CLas and a reservoir for additional infection. Basic sanitation was not adequately prioritized, with growers unwilling to destroy infected trees and orchards for the benefit of the greater landscape-level agroecosystem. Greater plant diversity might have supported populations of natural enemies against the psyllid, and plant diversity plus a healthy level of soil organic matter might have supported a microbial community with antagonistic capacity toward CLas. Only now are Florida growers looking for alternative crops, going as far as trials of the dry-climate crop pomegranate, an effort that was plagued with fungal wood canker diseases.

Of course the economic system played a role. Industrial production demands low diversity, high uniformity, concentrated resources, and substitution of capital intensive inputs over agroecological management. Growers will maximize individual benefit by retaining infected trees and harvesting sour deformed fruit for the juice market in order to recoup some of their investment. And in a perverse dynamic of the system, there are rich landowners who will retain unproductive trees on their property in order to classify their land as agricultural and qualify for government benefits. These growers are uninterested in the wellbeing of their trees or the industry as a whole, and from the perspective of industry itself they are wrecking any coordinated plan for eradicating the psyllid through spraying. With just one non-compliant grower, the psyllid finds refuge and can re-establish in the surrounding orchards, and thus the economics beats even conventional agriculture’s trump card.

The Asian citrus psyllid has already become established across a wide swath of California, but so far only a couple instances of HLB have been discovered in the Los Angeles area, out of ten thousand samples tested last year alone. The infected trees were destroyed, and movement of citrus material out of the zones of quarantine surrounding them is strictly prohibited, but unfortunately the psyllids will not be observing the quarantine boundaries. Researchers are scrambling to find resistant citrus germplasm for breeding resistant crop genotypes. New diagnostic tools are being developed for early detection that will register infection in sap samples from any part of an infected tree. Proponents of genetic engineering are scolding that their technology will have to be deployed to address conventional agriculture’s colossal wipeout on the technology treadmill it was already on.

One bright spot in the efforts to protect citrus in California is the work of the aforementioned Dr. Vidalakis. He is in charge of clearing all the citrus imports that are held in quarantine. Thanks to the foresight of policy makers in the 1930s, direct importation of citrus into the US is prohibited. Instead, all citrus material that someone wants to bring to the US passes through Vidalakis’ facility. From every sample of budwood his technicians painstakingly collect the microscopic growing tip, a piece of tissue out of reach of the plant’s sap and therefore of CLas or any sap-inhabiting viruses. They graft the tip onto a test plant, where it grows out and gets tested for all known viruses and bacterial pathogens, and also grafted to very susceptible plants that would presumably show symptoms in case of unknown viruses. Within a matter of months the importer receives certified virus- and CLas-free budwood, and citrus trees across the state are protected from devastating epidemics.

An admirable aspect of Vidalakis’ work is that he takes all comers. Immigrants from Asia can collect cuttings from their favorite citrus tree growing in their grandmother’s garden and submit them for high-tech cleanup. Vidalakis is not an agroecologist or social equity campaigner, but as a plant pathologist he recognizes that small-scale and backyard citrus growers are a legitimate component of the otherwise highly capitalized statewide citrus agroecosystem. If the small growers were marginalized, they would become the weak link in the protection of an entire industry.

Will the California citrus industry escape destruction from huanglongbing? It’s a cliffhanger. If industrial citrus production is able to overcome this agroecological reckoning, will it continue to present a sea of low diversity vegetation, a ready resource for the next intractable pest or pathogen from overseas or newly evolved domestically? Or will visionaries, a movement, and socioeconomic change arise and incorporate citrus production into a sustainable agricultural system designed using agroecological principles? There is never a bad time to turn to agroecology.

Plant pathologists have a sense of mission.  Take Ioannis Stergiopoulos.  Professor Stergiopoulos studies sigatoka disease of banana.  In case you are inclined to dismiss bananas as just a snack food, Stergiopoulos is ready point out that bananas are one of the top five staple crops in the world.  However, because they are clonally propagated, the world banana crop is dominated by a single variety and thus particularly vulnerable to potential emerging diseases.  Stergiopoulos also points out that pathogenic fungi in general are an emerging threat as they evolve new virulence genes.

 

Sigatoka is a complex of three diseases caused by closely related fungi.  Yellow sigatoka, caused by the fungus Pseudocercospora musae (P. musae for short), has been known for over a century.  Black sigatoka, caused by P. fijiensis, was discovered in 1963.  Eumusae leaf spot, caused by P. eumusae, was discovered the most recently, in the mid-1990s.  There is a progression of aggressiveness in the three species.  When black sigatoka arrives in a country that has only yellow sigatoka, it effectively displaces it, and then eumusae does the same with black sigatoka.  Black sigatoka can infect banana cultivars that are resistant to yellow sigatoka, and eumusae can infect cultivars resistant to sigatoka of either color (technically, to satisfy the plant pathologists, it is the pathogen that does the infecting, e.g. P. musae, and the disease is the result, e.g. yellow sigatoka; I will use “black sigatoka” as an abbreviation for “the black sigatoka pathogen”, etc.).  And while black sigatoka currently causes the biggest yield losses of the three, eumusae, which has not yet encircled the globe, is in a class with black sigatoka in terms of virulence.

 

Where do such diseases come from?  Stergiopoulos addresses that question using his extensive tool kit of genomic techniques, with which he can look at all the DNA that each species possesses and dig out trends in the genes.  His team analyzed mutations in 46 genes that are common to all species in the class of fungi that the three pathogens belong to, genes that seem to be important enough that they evolve very slowly.  This analysis showed that while the three belong to a single lineage, black sigatoka branched off first, while the other branch gave rise to yellow sigatoka and eumusae later.  They then looked at the family tree of these three plus other members of the class (remember that a class contains many orders and an order contains many families — maybe that would make it a class tree?) and overlaid the tree on the timeline from the first appearance of the class in geologic time in order to date the branches.  Black sigatoka branched off between 30 and 40 million years ago, while the other branch split into yellow sigatoka and eumusae lineages between 17 and 23 million years ago.  So not only does black sigatoka predate yellow, the reverse of their appearance in banana plantations, but all three predate the 20th century by more than a little.  So why the delay?

 

Of course there were probably other lineages that were branching off all this time — why should only these three species have become pathogenic?  Quite likely they were not pathogenic or else possessed little virulence when they first split off.  Pathogens have to acquire or adapt genes that let them take advantage of hosts.  Stergiopoulos’ analysis is able to give an idea of just how.

 

The three species’ genomes were found to contain a large proportion of transposable elements.  These are strings of DNA that contain genes that will copy the information in their own DNA string to another place in the genome.  This kind of random opportunistic jumping of segments of DNA to new sites tends to play havoc with the existing set of genes, but it can also occasionally cause advantageous outcomes.  The transposable elements can cause duplication of various genes, and sometimes the duplicate genes can evolve to take on new functions.

 

For a fungus to be a pathogen at all, it has to overcome a host plant’s defenses.  It does this with proteins called effectors, which disable components of the plant’s defense system.  A fungus can have the genes to produce a suite of different effectors, each one capable of taking on a different strategy that the plant can muster.  An expanded suite of effectors that can each evolve individually can be to the fungus’ advantage.  Stergiopoulos’ team found over 100 genes in each of the three sigatoka pathogens that show the genetic signature of effectors, and for each species about half of these genes arose after the lineages separated, quite possibly through evolution of duplicated effector genes.  Every time one of these effectors evolves to a point where it knocks out a host defense, the fungus gains an incremental advantage in growing and reproducing at the plant’s expense.

 

A pathogen also needs to be able to use the host’s resources for its own growth and reproduction.  A key aspect of this resource hijacking is the ability to digest the host’s cell walls.  The team found that black sigatoka and eumusae have had duplications of many of the same genes used for cell wall digestion, and this was a result of pure coincidence.  This parallel evolution is in some sense an adaptation to the host plant.  An increase in virulence afforded by enhanced cell wall digesting ability could also allow the fungi to grow and spread more easily, which we would then come to our attention as an emerging disease.

 

The team wanted to know what other genes might be different between yellow sigatoka on the one hand and the more virulent species on the other, in order to get a fuller picture of the traits that make a fungus more virulent.  They compared the three species’ genes to annotated lists of genes of known function in all eukaryotes (plants, animals, fungi, protozoans, etc.), paying special attention to genes that had gotten duplicated.  The result that popped out was an increase in copies in black sigatoka and eumusae of genes associated with metabolism — genes for transport and metabolism of amino acids, fats, carbohydrates, and secondary metabolites and genes for energy use.  Since the two species have achieved higher virulence, the team believes that an increase in pathways for metabolism is key for virulence.  One could imagine that when cell-wall-digesting enzymes liberate a plant cell’s juices, a fungus that has greater capacity for handling the spoils would insure that more of the goodies go toward its own growth and reproduction, rather than letting nearby opportunistic fungi take advantage of them.

 

Thus, the Stergiopoulos team has done a magnificent job of presenting the How of the evolution of virulence — gene duplications, evolution of effectors, increased ability to digest cell walls, and increased capacity to use the resources liberated.  What is outside of their purview is the Why.  Why should three species that have been evolving for millions of years all turn virulent in the 20th century?  Researchers who love mining genomes for scientific treasures will use plant pathogens as prospecting grounds, and they will justify their intellectual pursuits to funding agencies by promising insights into developing targeted disease control methods.  Meanwhile the environmental and economic factors that lead to the emergence of new pathogens are no secret to molecular plant pathologists, but they are just not as interesting to people attracted to the minutiae of genetic information.

 

And what are these factors?  Environmental factors include monocropping, sequential cropping of the same species, low genetic diversity, and movement of plant material across continents and oceans, all the product of human intervention.  Bananas are a special case, being sterile triploids that present problems for breeding, and being propagated from side shoots that can be planted across fields and countries leading to essentially one big banana plant with zero diversity divided up into multiple stalks across the landscape.  When a fungus can grow unimpeded over a vast area year after year, every cell division and every mating is an opportunity to evolve to better take advantage of a plentiful host.  When infected material is transported by long-distance travelers, a previously unknown disease from the Sigatoka District of Fiji can end up with a worldwide distribution.

 

However, many of the factors underlying the environmental are the economic.  Corporations seeking to make money selling a product find an agricultural commodity that is easy to produce, tolerates long-distance shipping, and presents a uniform quality that shoppers expect on supermarket shelves, they plant it in machine-harvestable rows at the maximum density, they fertilize it into a succulent treat for a fungus, and they promote it in extensive advertising campaigns that make an exotic tropical fruit seem like a necessary addition to a bowl of cereal in a country without a banana industry.  The profit motive overrides environmental and phytopathological considerations.

 

With this backdrop, the efforts of molecular plant pathologists can actually serve to consolidate corporate dominance of agriculture.  Moneyed interests recruit scientists to find high-investment technologies that will favor the biggest growers.  Plant pathologists deceive themselves into believing they are feeding the world, when they are actually propping up corporate profits, leaving the hungry still hungry.  Even the claim of saving a widely grown staple crop is equivocal, with a significant portion of the world harvest being industrially produced by multinational corporations for export.

 

We need scientists who are experts on plant diseases who can aid us in diagnosing our crops, advise us on designing our agroecosystems, assist our efforts in harnessing crop evolution, and warn us about emerging threats.  But when food becomes a commodity, scientific expertise becomes captured and misdirected.  What would an economic system look like where food is not a commodity?  It will take many minds to work out all the details, but it probably will not include a banana on your daily bowl.